Chemokine Signaling Directs Trunk Lymphatic Network Formation along the Preexisting Blood Vasculature

Developmental Cell

Volumn 22, Issue 4, 2012, Pages 824-836

  Cha, Young Ryun ^a   Fujita, Misato ^a   Butler, Matthew ^a   Isogai, Sumio ^b   Kochhan, Eva ^c   Siekmann, Arndt F ^c   Weinstein, Brant M ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b IWATE MEDICAL UNIVERSITY   (Japan)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE LIGAND CXCL12A; CHEMOKINE LIGAND CXCL12B; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCR4A; CHEMOKINE RECEPTOR CXCR4B; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; LOSS OF FUNCTION MUTATION; LYMPH VESSEL ENDOTHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; CELL COMMUNICATION; CELLS, CULTURED; CHEMOKINE CXCL12; CHEMOKINES, CXC; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; LYMPHATIC SYSTEM; RECEPTORS, CXCR4; RECOMBINATION, GENETIC; RNA PROBES; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84859809053     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.01.011     Document Type: Article

References (64)

1. Achen M.G., McColl B.K., Stacker S.A. Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 2005, 7:121-127.
2. Alitalo K., Tammela T., Petrova T.V. Lymphangiogenesis in development and human disease. Nature 2005, 438:946-953.
3. Bouvrée K., Larrivée B., Lv X., Yuan L., DeLafarge B., Freitas C., Mathivet T., Bréant C., Tessier-Lavigne M., Bikfalvi A., et al. Netrin-1 inhibits sprouting angiogenesis in developing avian embryos. Dev. Biol. 2008, 318:172-183.
4. Bussmann J., Bos F.L., Urasaki A., Kawakami K., Duckers H.J., Schulte-Merker S. Arteries provide essential guidance cues for lymphatic endothelial cells in the zebrafish trunk. Development 2010, 137:2653-2657.
5. Bussmann J., Wolfe S.A., Siekmann A.F. Arterial-venous network formation during brain vascularization involves hemodynamic regulation of chemokine signaling. Development 2011, 138:1717-1726.
6. Butler M.G., Isogai S., Weinstein B.M. Lymphatic development. Birth Defects Res. C Embryo Today 2009, 87:222-231.
7. Chong S.W., Nguyet L.M., Jiang Y.J., Korzh V. The chemokine Sdf-1 and its receptor Cxcr4 are required for formation of muscle in zebrafish. BMC Dev. Biol. 2007, 7:54.
8. Christie T.L., Carter A., Rollins E.L., Childs S.J. Syk and Zap-70 function redundantly to promote angioblast migration. Dev. Biol. 2010, 340:22-29.
9. Covassin L.D., Siekmann A.F., Kacergis M.C., Laver E., Moore J.C., Villefranc J.A., Weinstein B.M., Lawson N.D. A genetic screen for vascular mutants in zebrafish reveals dynamic roles for Vegf/Plcg1 signaling during artery development. Dev. Biol. 2009, 329:212-226.
10. David N.B., Sapède D., Saint-Etienne L., Thisse C., Thisse B., Dambly-Chaudière C., Rosa F.M., Ghysen A. Molecular basis of cell migration in the fish lateral line: role of the chemokine receptor CXCR4 and of its ligand, SDF1. Proc. Natl. Acad. Sci. USA 2002, 99:16297-16302.
11. Del Giacco L., Pistocchi A., Ghilardi A. prox1b Activity is essential in zebrafish lymphangiogenesis. PLoS ONE 2010, 5:e13170.
12. Doitsidou M., Reichman-Fried M., Stebler J., Köprunner M., Dörries J., Meyer D., Esguerra C.V., Leung T., Raz E. Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 2002, 111:647-659.
13. Ertzer R., Müller F., Hadzhiev Y., Rathnam S., Fischer N., Rastegar S., Strähle U. Cooperation of sonic hedgehog enhancers in midline expression. Dev. Biol. 2007, 301:578-589.
14. Esengil H., Chang V., Mich J.K., Chen J.K. Small-molecule regulation of zebrafish gene expression. Nat. Chem. Biol. 2007, 3:154-155.
15. Fujita M., Cha Y.R., Pham V.N., Sakurai A., Roman B.L., Gutkind J.S., Weinstein B.M. Assembly and patterning of the vascular network of the vertebrate hindbrain. Development 2011, 138:1705-1715.
16. Geudens I., Herpers R., Hermans K., Segura I., Ruiz de Almodovar C., Bussmann J., De Smet F., Vandevelde W., Hogan B.M., Siekmann A., et al. Role of delta-like-4/Notch in the formation and wiring of the lymphatic network in zebrafish. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1695-1702.
17. Ghysen A., Dambly-Chaudière C. The lateral line microcosmos. Genes Dev. 2007, 21:2118-2130.
18. Gray H. Anatomy of the Human Body 1918, Lea & Febiger, Philadelphia.
19. Haas P., Gilmour D. Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev. Cell 2006, 10:673-680.
20. Hauptmann G., Gerster T. Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos. Trends Genet. 1994, 10:266.
21. Hogan B.M., Bos F.L., Bussmann J., Witte M., Chi N.C., Duckers H.J., Schulte-Merker S. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet. 2009, 41:396-398.
22. Hollway G.E., Bryson-Richardson R.J., Berger S., Cole N.J., Hall T.E., Currie P.D. Whole-somite rotation generates muscle progenitor cell compartments in the developing zebrafish embryo. Dev. Cell 2007, 12:207-219.
23. Isogai S., Horiguchi M., Weinstein B.M. The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev. Biol. 2001, 230:278-301.
24. Isogai S., Lawson N.D., Torrealday S., Horiguchi M., Weinstein B.M. Angiogenic network formation in the developing vertebrate trunk. Development 2003, 130:5281-5290.
25. Issa A., Le T.X., Shoushtari A.N., Shields J.D., Swartz M.A. Vascular endothelial growth factor-C and C-C chemokine receptor 7 in tumor cell-lymphatic cross-talk promote invasive phenotype. Cancer Res. 2009, 69:349-357.
26. Kamei M., Weinstein B.M. Long-term time-lapse fluorescence imaging of developing zebrafish. Zebrafish 2005, 2:113-123.
27. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
28. Knaut H., Werz C., Geisler R., Nüsslein-Volhard C. A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 2003, 421:279-282. Tübingen 2000 Screen Consortium.
29. Küchler A.M., Gjini E., Peterson-Maduro J., Cancilla B., Wolburg H., Schulte-Merker S. Development of the zebrafish lymphatic system requires VEGFC signaling. Curr. Biol. 2006, 16:1244-1248.
30. Larrivée B., Freitas C., Trombe M., Lv X., Delafarge B., Yuan L., Bouvrée K., Bréant C., Del Toro R., Bréchot N., et al. Activation of the UNC5B receptor by Netrin-1 inhibits sprouting angiogenesis. Genes Dev. 2007, 21:2433-2447.
31. Lauderdale J.D., Davis N.M., Kuwada J.Y. Axon tracts correlate with netrin-1a expression in the zebrafish embryo. Mol. Cell. Neurosci. 1997, 9:293-313.
32. Lawson N.D., Weinstein B.M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 2002, 248:307-318.
33. Lawson N.D., Mugford J.W., Diamond B.A., Weinstein B.M. phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 2003, 17:1346-1351.
34. Lim A.H., Suli A., Yaniv K., Weinstein B., Li D.Y., Chien C.B. Motoneurons are essential for vascular pathfinding. Development 2011, 138:3847-3857.
35. McKinney M.C., Weinstein B.M. Chapter 4. Using the zebrafish to study vessel formation. Methods Enzymol. 2008, 444:65-97.
36. Melani M., Weinstein B.M. Common factors regulating patterning of the nervous and vascular systems. Annu. Rev. Cell Dev. Biol. 2010, 26:639-665.
37. Müller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., McClanahan T., Murphy E., Yuan W., Wagner S.N., et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
38. Nair S., Schilling T.F. Chemokine signaling controls endodermal migration during zebrafish gastrulation. Science 2008, 322:89-92.
39. Navankasattusas S., Whitehead K.J., Suli A., Sorensen L.K., Lim A.H., Zhao J., Park K.W., Wythe J.D., Thomas K.R., Chien C.B., Li D.Y. The netrin receptor UNC5B promotes angiogenesis in specific vascular beds. Development 2008, 135:659-667.
40. Ny A., Koch M., Schneider M., Neven E., Tong R.T., Maity S., Fischer C., Plaisance S., Lambrechts D., Héligon C., et al. A genetic Xenopus laevis tadpole model to study lymphangiogenesis. Nat. Med. 2005, 11:998-1004.
41. Oliver G., Alitalo K. The lymphatic vasculature: recent progress and paradigms. Annu. Rev. Cell Dev. Biol. 2005, 21:457-483.
42. Pedrioli D.M., Karpanen T., Dabouras V., Jurisic G., van de Hoek G., Shin J.W., Marino D., Kälin R.E., Leidel S., Cinelli P., et al. miR-31 functions as a negative regulator of lymphatic vascular lineage-specific differentiation in vitro and vascular development in vivo. Mol. Cell. Biol. 2010, 30:3620-3634.
43. Provost E., Rhee J., Leach S.D. Viral 2A peptides allow expression of multiple proteins from a single ORF in transgenic zebrafish embryos. Genesis 2007, 45:625-629.
44. Raman D., Baugher P.J., Thu Y.M., Richmond A. Role of chemokines in tumor growth. Cancer Lett. 2007, 256:137-165.
45. Sabin F.R. On the origin of the lymphatic system from the veins and the development of the lymph hearts and thoracic duct in the pig. Am. J. Anat. 1902, 1:367-389.
46. Sabin F.R. The lymphatic system in human embryos, with a consideration of the morphology of the system as a whole. Am. J. Anat. 1909, 9:43-91.
47. Saharinen P., Helotera H., Miettinen J., Norrmen C., D'Amico G., Jeltsch M., Langenberg T., Vandevelde W., Ny A., Dewerchin M., et al. Claudin-like protein 24 interacts with the VEGFR-2 and VEGFR-3 pathways and regulates lymphatic vessel development. Genes Dev. 2010, 24:875-880.
48. Siekmann A.F., Standley C., Fogarty K.E., Wolfe S.A., Lawson N.D. Chemokine signaling guides regional patterning of the first embryonic artery. Genes Dev. 2009, 23:2272-2277.
49. Somasundaram R., Herlyn D. Chemokines and the microenvironment in neuroectodermal tumor-host interaction. Semin. Cancer Biol. 2009, 19:92-96.
50. Suster M.L., Sumiyama K., Kawakami K. Transposon-mediated BAC transgenesis in zebrafish and mice. BMC Genomics 2009, 10:477.
51. Szymczak A.L., Workman C.J., Wang Y., Vignali K.M., Dilioglou S., Vanin E.F., Vignali D.A. Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector. Nat. Biotechnol. 2004, 22:589-594.
52. Tamamura H., Hiramatsu K., Mizumoto M., Ueda S., Kusano S., Terakubo S., Akamatsu M., Yamamoto N., Trent J.O., Wang Z., et al. Enhancement of the T140-based pharmacophores leads to the development of more potent and bio-stable CXCR4 antagonists. Org. Biomol. Chem. 2003, 1:3663-3669.
53. Tamamura H., Hori A., Kanzaki N., Hiramatsu K., Mizumoto M., Nakashima H., Yamamoto N., Otaka A., Fujii N. T140 analogs as CXCR4 antagonists identified as anti-metastatic agents in the treatment of breast cancer. FEBS Lett. 2003, 550:79-83.
54. Tammela T., Alitalo K. Lymphangiogenesis: Molecular mechanisms and future promise. Cell 2010, 140:460-476.
55. Tilney N.L. Patterns of lymphatic drainage in the adult laboratory rat. J. Anat. 1971, 109:369-383.
56. Torres-Vázquez J., Gitler A.D., Fraser S.D., Berk J.D., Pham V.N., Fishman M.C., Childs S., Epstein J.A., Weinstein B.M. Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev. Cell 2004, 7:117-123.
57. Valentin G., Haas P., Gilmour D. The chemokine SDF1a coordinates tissue migration through the spatially restricted activation of Cxcr7 and Cxcr4b. Curr. Biol. 2007, 17:1026-1031.
58. Wang Y., Oliver G. Current views on the function of the lymphatic vasculature in health and disease. Genes Dev. 2010, 24:2115-2126.
59. Warming S., Costantino N., Court D.L., Jenkins N.A., Copeland N.G. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res. 2005, 33:e36.
60. Westerfield M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio) 2000, University of Oregon Press, Eugene, OR. Fourth Edition.
61. Wigle J.T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778.
62. Wiley H.E., Gonzalez E.B., Maki W., Wu M.T., Hwang S.T. Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma. J. Natl. Cancer Inst. 2001, 93:1638-1643.
63. Wilson B.D., Ii M., Park K.W., Suli A., Sorensen L.K., Larrieu-Lahargue F., Urness L.D., Suh W., Asai J., Kock G.A., et al. Netrins promote developmental and therapeutic angiogenesis. Science 2006, 313:640-644.
64. Yaniv K., Isogai S., Castranova D., Dye L., Hitomi J., Weinstein B.M. Live imaging of lymphatic development in the zebrafish. Nat. Med. 2006, 12:711-716.